The carob tree (Ceratonia siliqua L.) is an evergreen shrub or tree cultivated in the Mediterranean area for its sugar-rich pods and gum-containing seeds. It reaches a height of 8-17 m in the wild but cultivated trees are smaller. It has a broad hemispherical crown, a thick trunk and sturdy branches (Ecocrop, 2011; Battle et al., 1997). The carob tree has an extensive root system with a deep taproot and lateral roots. Its leaves are alternate, pinnate, with or without terminal leaflets, and 10-20 cm long. The dark green leaflets have a very thick epidermis containing large amounts of tannins (Shepperd, 2008). Each tree bears both female and male, or hermaphroditic, flowers (some cultivars may be completely hermaphroditic): plantations should comprise about 12% of pollinators (male or hermaphroditic trees) (Battle et al., 1997; Göhl, 1982). The small and numerous flowers are borne in clusters that grow directly along the branches (Battle et al., 1997). The fruit is an indehiscent straight or curved pod, 10-30 cm long, 1.5-3.5 cm broad and 6-20 mm thick. The pods have a wrinkled surface that turns dark brown and leathery at maturation. They contain 5 to 18 hard brown seeds (10% of the pod weight) embedded in a sweet thick pulpy substance (Shepperd, 2008; Battle et al., 1997). The seeds, all being the same size, are used as weights in eastern Mediterranean countries: the word "carat" comes from qīrāṭ (قيراط), the Arabic name of the seeds (Göhl, 1982).

The carob tree is a very useful resource. Traditionally, carob pulp has been used for food: roasted and eaten as a snack, roasted and ground to make a cocoa substitute, fermented to make alcohol, or diluted to make carob syrup (Battle et al., 1997). The pods themselves are used as a famine food, as the tree survives and keeps fruiting during periods of scarcity (Freedman, 2009). The most important industrial carob product today is the carob gum, a galactomannan extracted from the seeds (or beans), which is a common food thickener and stabilizer. Feed products derived from the carob trees are the whole ground pods which can be fed to ruminants and non-ruminants, the dried, deseeded sugar-rich pulp, and the carob germ meal (the by-product of gum extraction). Carob leaves are relished by browsing livestock (Battle et al., 1997).

Carob trees also provide a wood used for making utensils and slow-burning charcoal (Shepperd, 2008) and extracted to yield algarrobin, a textile dyeing agent (Morton, 1987). Carob trees are used as an ornamental evergreen species and are helpful in afforestation (Battle et al., 1997).

Note on terminology

There are four main carob feed products: whole carob pods, carob pulp (carob kibbles, deseeded carob pods), carob germs (carob germ meal) and the less common carob seeds. The terms carob pod meal and carob bean meal used in the literature often refer to both the whole pods and the deseeded pods (and possibly the germ meal to some extent). The term bean is particularly confusing because it concerns the whole pod and not just the seeds. Likewise, the term carob bean husks may refer to the deseeded pod (including the pulp), rather than just the pod covering.

Distribution

The carob tree originated from the Middle-East (Turkey, Syria) and was brought by human movement to Greece and Italy, along the North African coast and northwards into Spain and Portugal. It is now an important tree species in the coastal areas of the Mediterranean Basin as it is well adapted to summer drought periods and to the poor calcareous soils of this area (Battle et al., 1997). It is generally found within 30-45°N and 30-40°S and from sea level to an altitude of 500-1000 m (Ecocrop, 2011; Orwa et al., 2009; Battle et al., 1997). Ceratonia siliqua prefers mild winters and hot dry summers. It has low cold tolerance and some 5000 to 6000 hours above 9°C are necessary for pods to ripen. However, the carob tree can resist frost down to -6°C (Battle et al., 1997).

A slow-growing species, the carob tree may live more than a 100 years and begins fruiting after 6 or 7 years of growth. The carob tree is drought-hardy and can grow in places with annual rainfall as low as 250-500 mm, though a minimum of 500-550 mm and irrigation is required for commercial production. Carob trees are dew-sensitive and develop only in places where there are less than 220 dew nights per annum (Ecocrop, 2011). Carob trees can grow on a wide range of soils, and are saline tolerant up to 3% NaCl in the soil, but they prefer sandy well-drained loams or calcareous soils with a high lime content (Battle et al., 1997). Carob trees are resistant to termites, heat and fire. They cannot withstand strong winds and waterlogged conditions (Orwa et al., 2009; Battle et al., 1997).

In 2010 it was estimated that there were about 92,000 ha worldwide planted with carob trees, producing a total of 153,000 t of carob beans. Spain and Italy accounted for 50% of the production, followed by Morocco, Portugal, Turkey and Greece (FAO, 2011). Average worldwide yield is 1.7 t/ha (FAO, 2011) but modern production can reach yields of 5-7 t/ha (Battle et al., 1997).

Processes

Carob pods are removed manually or mechanically from the branches and collected in nets placed under the trees. Harvesting must be done carefully to avoid damaging the next year's flowers, which are fragile and close to the ripe pods. The fallen pods are air-dried for 48-72 h in a ventilated area (Shepperd, 2008; Battle et al., 1997). Once dried (about 92% DM), the pods are brought to the processing plant where they are crushed to separate the seeds from the pulp. The pulp is ground to different sizes depending on the end market (feed or food) (Battle et al., 1997). For animal feeding, whole pods may also be hammer-milled into carob bean flour or carob bean meal. The seeds have a hard coat that must be removed by acid treatment or roasting. The dehulled seeds are then split into endosperm, which is ground to produce gum, and germs, which are ground and dried to make carob germ meal (Battle et al., 1997).

Environmental impact

N fixing legume

Carob was long believed to be unable to fix nitrogen, but bacteria thought to belong to the Rhizobium genus have been isolated from carob root nodules (El Idrissi et al., 1996).

Agricultural diversification, afforestation and soil erosion control

The carob tree, being hardy, drought- and salt-tolerant, with low orchard management requirements (which allow part-time farming) is a good candidate for agriculture diversification in semi-arid coastal areas. Carob trees may also be helpful in degraded areas threatened by soil erosion and desertification (Battle et al., 1997).

Other environmental services

Carob trees are used as windbreaks around orchards. Because of their dense foliage, they are also helpful buffers against noise from factories, roads and railways (Battle et al., 1997).

Nutritional aspects

Nutritional attributes

Carob pods and other carob products are valuable feeds, but as noted in Potential constraints below, their inclusion in animal diets may be limited by their tannin content.

Carob pods

Carob pods are a source of non-structural carbohydrates (about 45% DM) and therefore of energy. These sugars consist mostly of sucrose (Battle et al., 1997), which makes the pods highly palatable for most animal species. Some authors also report large amounts of glucose (Ayaz et al., 2007). Carob pods are a poor source of protein (about 5% DM) with a low lysine content (< 4% of the protein). Fat content is also low (< 1%). Carob lipids are rich in oleic and lineoleic (18:1 and 18:2) fatty acids (Gubbuk et al., 2010). Carob pods have a high fibre content (33% NDF, 31% ADF DM). The lignin content is particularly important (8-25% DM). One reason for the close NDF and ADF value may be that the method of determination of ADF may have caused some kind of polymerization of sugars with the fibre fraction resulting in an artificial increase in apparent ADF content (Milad et al., 2010). Crude fibre content is very low (9% DM) when compared to NDF and ADF. This difference and the large variability in ADF and lignin content could be explained by the presence of tannins, as tannin-protein complexes may be detected as artificial fibre (Silanikove et al., 2006). NDF, ADF, ADL and crude fibre contents are positively and significantly related. Cell wall constituents and crude protein are not correlated with the soluble sugars contents.

Carob germ meal

Carob germ meal is a high-protein ingredient (50% DM) with a better protein quality (lysine > 5% protein) than pod meal. It contains more fat (> 5%) but much less fibre (< 5% crude fibre) than the pods.

These tannins interfere with protein digestibility and may reduce the digestibility of other feeds used together with carob, thus reducing body weight gains (Calixto et al., 1982). The presence of tannins in carob pods has been shown to have deleterious effects on digestion, growth and milk production in ruminants, and growth in poultry (Silanikove et al., 2006). One proposed mechanism of action specific to carob tannins is that they trap fat and cholesterol, causing unwanted cholesterol excretion and resulting in hypercholesterolemia. Supplementation with PEG (polyethylene glycol) helps to release the cholesterol, thus countering this effect (Silanikove et al., 2006).

However, it should be noted that carob tannins also have anti-diarrheic properties and that toasted carob powder is used to that effect in children (Lizardo et al., 2002).

Palatability

In green non-ripe pods, condensed tannins cause a strong astringency taste in the mouth, making the pods unpalatable. This astringency decreases during ripening, due the polymerization and condensation of tannins, making the ripe pod more palatable (Silanikove et al., 2006). Also, carob pods contain free iso-butyric acid (about 0.6-0.9% DM) that give them a specific cheese-like odour, which may have positive or negative consequences on palatability (Berna et al., 1997). However, much lower values (<0.05% DM) have been reported for deseeded pods (Iipumbu, 2008).

Ruminants

Carob pods

Carob pods contain large amounts of sugars, which makes them a good source of energy and very palatable. Carob bean meal has been used as a substitute for grain in the diets of ruminants. Carob pods may be beneficial as a supplement for ruminants under critical feeding conditions (Hall et al., 1977). However, protein supplementation is required when high amounts of carob pods are included into ruminant diets. While tannins can have positive effects on ruminant diets because they increase the bypass protein content (Aharoni et al., 1998), carob tannins are known to be detrimental to growth in ruminants.

Nutritive value

Estimations of the digestibility of carob pods vary widely between references. The CIHEAM tables report an OM digestibility value of 59% (Alibes et al., 1990) while the INRA-AFZ tables give 70% (Sauvant et al., 2004). Carob trials tend to report the digestibility of mixed diets rather than the digestibility of carob pods alone: from one of these experiments, it is possible to calculate an OMD value of 74% (Obeidat et al., 2011). Values of 74-75% estimated by the gas production method have been reported for both the whole pods and kibbles (Karabulut et al., 2006). The OM digestibility (%) of carob pods can also be predicted from crude fibre (CF, % DM):

OM digestibility = 78.1 - 1,73 CF (n=7, R²=48%, RSD=9.3)

Based on this equation, the mean crude fibre content of 9.0% DM corresponds to an OMD of 63% (close to the CIHEAM value) and to an ME content of 9.6 MJ/kg DM. Carob pod meal is less digestible than other feeds with a similar crude fibre, which may be explained by the detrimental effect of carob tannins on digestibility. High OM digestibility values such as the one reported in the INRA-AFZ tables are probably overestimated.

Growing sheep and goats

Inclusion levels in the 20-25% range seem to be appropriate for growing sheep and goats. The replacement of barley grain by carob pods up to 25% in fattening Awassi lambs did not affect feed intake, growth performance, carcass characteristics and meat quality. Diet digestibility was only slightly affected by increasing the inclusion rate of carob pods from 12.5% to 25% (Obeidat et al., 2011). However, condensed tannins from carob pulp can be detrimental to feed digestibility and growth performance (Priolo et al., 2000). In Comisana lambs, feeding a diet containing 20% carob pulp in replacement of barley did not affect live weight and most meat quality parameters but resulted in a higher feed intake and a depressed feed conversion ratio (Priolo et al., 1998). Anglo-Nubian kids fed 52% carob pods performed very poorly, with reduced growth rates (-40%) and poor conversion ratios (Silanikove et al., 2006).

Treatment with PEG (polyethylene glycol) has been proved as an effective mean to counteract the negative effects of tannins. For example the inclusion of 4% PEG in a diet containing 56% of carob pod meal resulted in performance and meat quality similar to the one obtained with the maize-based control diet (Priolo et al., 2000). Similar results have been observed on kids (3.3% PEG, 52% carob meal, Silanikove et al., 2006). Lambs and kids fed high-tannin diets containing carob pulp have a lighter longissimus muscle colour, an effect that is again corrected by PEG supplementation. This effect could be linked with a reduced myoglobin synthesis although iron absorption seemed not to be affected by condensed tannins in sheep (Priolo et al., 2004).

Carob kibbles can be associated with ammoniated straw (45% and 40% of diet DM respectively) as supplementary sources of N for the rumen ecosystem (Milad et al., 2010).

Ewes and lactating goats

It was estimated that carob pods contain sufficient crude protein and energy to meet the maintenance and lactation requirements of ewes in semi-arid rangelands (El-Shatnawi et al., 2001). In dairy goats, a non-forage diet containing an adequate amount of structured fibre, contributed by carob pods (26%) and beet pulp (27%), could replace a ration based on poor quality forage (Rapetti et al., 2005).

Carob seeds

There is little information available on the use of carob seeds for ruminants. It was estimated that carob pods contain sufficient crude protein and energy to meet the maintenance and lactation requirements of ewes in semi-arid rangelands (El-Shatnawi et al., 2001). Gas production of carob seeds was found to be significantly lower than that of carob pods and kibbles, while the estimated OMD (79%) and ME value (11.6 MJ/kg DM) of carob seeds were significantly higher. However, the authors caution that the higher crude protein content of the seeds may have resulted in overestimation of OMD and ME (Karabulut et al., 2006).

Carob browse

In Ethiopia, carob foliage compared to 40 other tropical browse species was found to have a very low protein solubility, low DM and rumen degradable protein, coupled with very low values of DM and N disappearance in the intestine (Kaitho et al., 1998). Fibre digestibility significantly decreased in ewes fed carob leaves that contained high concentrations of tannins (Silanikove et al., 1996).

Pigs

There is limited information available on the use of carob products for pigs. Carob pod meal can be included up to 10-20% DM in pig diets. The high sugar content of carob pods makes them palatable and thus valuable to increase feed intake. They can replace other feeds with high sugar contents (dextrose, starch, milk powder) without adversely affecting feed intake (Kotrotsios et al., 2011). However, an inclusion rate of pod meal to 12.5% DM resulted in a significant decrease in nutrient digestibility during the weaning, growing and fattening periods (Kotrotsios et al., 2010). The depressive effect of carob pod meal on protein digestibility was noted in early trials (Becker et al., 1955).

Small amounts (up to 6%) of carob pod meal in piglet diets have been shown to sustain health and performance after weaning. The prevalence of post-weaning diarrhea tended to be 20% and 33% lower than the control at 3% and 6% inclusion rates respectively (Lizardo et al., 2002).

Poultry

There is limited information available on the use of carob products in poultry diets.

Carob pods

Poultry

The use of whole carob pods (including seeds) at an inclusion rate as low as 5% is detrimental to chicken performance (Kratzer et al., 1951). The negative effect of carob meal can be partially overcome when extra protein and/or energy is added to the diet (Kamarinou et al., 1979). For poultry the only available nutrient component seems to be the sugar, and poor results are obtained because of the bulkiness (Göhl, 1982).

Geese

In geese, apparent and true metabolizable energy values of carob pod meal were estimated at 6.1 and 6.6 MJ/kg respectively. The inclusion of up to 20% carob pod meal in the diet increased protein digestibility but a 30% inclusion rate resulted in deleterious effects on animal performance (Sahle et al., 1992).

Carob seeds

When seeds were introduced at low levels in poultry diets (6 and 9%), digestibility of protein and fat was markedly reduced by 13 to 30% and the viscosity of jejunal digesta was increased (Ortiz et al., 2004). As a consequence, carob seeds are regarded as unsuitable for poultry feeding.

Carob germs

Carob germs can be used up to 20% of the diet without supplementation in poultry diets with good results (Göhl, 1982).

The main nutritional interest of carob pods for rabbits is their high sugar content, which supplies a relatively high digestible energy content (9.00 MJ DE/kg as fed) unusual for a product containing a large amount of lignin (Villamide et al., 2010). This high lignin content is also beneficial to the fibre equilibrium required for the health of the rabbit's digestive tract (Gidenne et al., 2010). On the other hand, carob pods have a low protein content of poor quality, being clearly deficient in lysine and in sulphur-containing amino-acids when compared to the requirements for rabbits (Lebas 2004). Furthermore, estimations of protein digestibility vary widely, from 20% (Villamide et al., 2010) to 69% (Gasmi-Boubaker et al., 2008).

Whole carob pods

Whole carob pods are much used in Algeria as an ingredient, in small scale family rabbit units, in addition to wheat bran, particularly during summer and winter (Berchiche et al., 1994; Zerrouki, 2011). The high palatability of whole carob pods for rabbits has been noted (Morton, 1987).